Artículo

Artículo de Acceso Abierto. Puede ser descargado en su versión final
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

To gain insights into the natural variation of root hydraulics and its molecular components, genotypic differences related to root water transport and plasma membrane intrinsic protein (PIP) aquaporin expression were investigated in 13 natural accessions of Arabidopsis (Arabidopsis thaliana). The hydraulic conductivity of excised root systems (Lpr) showed a 2-fold variation among accessions. The contribution of aquaporins to water uptake was characterized using as inhibitors mercury, propionic acid, and azide. The aquaporin-dependent and -independent paths of water transport made variable contributions to the total hydraulic conductivity in the different accessions. The distinct suberization patterns observed among accessions were not correlated with their root hydraulic properties. Real-time reverse transcription-polymerase chain reaction revealed, by contrast, a positive overall correlation between Lpr and certain highly expressed PIP transcripts. Root hydraulic responses to salt stress were characterized in a subset of five accessions (Bulhary-1, Catania-1, Columbia-0, Dijon-M, and Monte-Tosso-0 [Mr-0]). Lpr was down-regulated in all accessions except Mr-0. In Mr-0 and Catania-1, cortical cell hydraulic conductivity was unresponsive to salt, whereas it was down-regulated in the three other accessions. By contrast, the five accessions showed qualitatively similar aquaporin transcriptional profiles in response to salt. The overall work provides clues on how hydraulic regulation allows plant adaptation to salt stress. It also shows that a wide range of root hydraulic profiles, as previously reported in various species, can be observed in a single model species. This work paves the way for a quantitative genetics analysis of root hydraulics. © 2011 American Society of Plant Biologists.

Registro:

Documento: Artículo
Título:Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions
Autor:Sutka, M.; Li, G.; Boudet, J.; Boursiac, Y.; Doumas, P.; Maurel, C.
Filiación:Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Universite, F-34060 Montpellier cedex 2, France
Diversité et Adaptation des Plantes Cultivées, Equipe Rhizogénese, UMR 188 Institut de Recherche pour le Developpement/INRA/Montpellier SupAgro/ Universite, F-34394 Montpellier cedex 5, France
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160 Piso 4 (C1428EGA), Buenos Aires, Argentina
Diversité et Ecophysiologie des Céréales, UMR 1095 INRA/Université Blaise Pascal, Campus des Cézeaux, 24 avenue des Landais, BP 80026, F-63171 Aubière, France
Palabras clave:aquaporin; messenger RNA; sodium chloride; water; Arabidopsis; article; drug effect; gene expression profiling; gene expression regulation; genetic variability; genetics; growth, development and aging; histology; metabolism; physiological stress; physiology; plant root; principal component analysis; Aquaporins; Arabidopsis; Gene Expression Profiling; Gene Expression Regulation, Plant; Genetic Variation; Plant Roots; Principal Component Analysis; RNA, Messenger; Sodium Chloride; Stress, Physiological; Water; Arabidopsis; Arabidopsis thaliana
Año:2011
Volumen:155
Número:3
Página de inicio:1264
Página de fin:1276
DOI: http://dx.doi.org/10.1104/pp.110.163113
Handle:http://hdl.handle.net/20.500.12110/paper_00320889_v155_n3_p1264_Sutka
Título revista:Plant Physiology
Título revista abreviado:Plant Physiol.
ISSN:00320889
CODEN:PLPHA
CAS:aquaporin, 215587-75-0; sodium chloride, 7647-14-5; water, 7732-18-5; Aquaporins; RNA, Messenger; Sodium Chloride, 7647-14-5; Water, 7732-18-5
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00320889_v155_n3_p1264_Sutka.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00320889_v155_n3_p1264_Sutka

Referencias:

  • Ache, P., Bauer, H., Kollist, H., Al-Rasheid, K.A., Lautner, S., Hartung, W., Hedrich, R., Stomatal action directly feeds back on leaf turgor: New insights into the regulation of the plant water status from non-invasive pressure probe measurements (2010) Plant J, 62, pp. 1072-1082
  • Alexandersson, E., Danielson, J.A., Råde, J., Moparthi, V.K., Fontes, M., Kjellbom, P., Johanson, U., Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress (2010) Plant J, 61, pp. 650-660
  • Alexandersson, E., Fraysse, L., Sjövall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., Johanson, U., Kjellbom, P., Whole gene family expression and drought stress regulation of aquaporins (2005) Plant Mol Biol, 59, pp. 469-484
  • Alonso-Blanco, C., Aarts, M.G., Bentsink, L., Keurentjes, J.J., Reymond, M., Vreugdenhil, D., Koornneef, M., What has natural variation taught us about plant development, physiology, and adaptation? (2009) Plant Cell, 21, pp. 1877-1896
  • Aroca, R., Tognoni, F., Irigoyen, J.J., Sanchez-Diaz, M., Pardossi, A., Different root low temperature response to two maize genotypes differing in chilling sensitivity (2001) Plant Physiol Biochem, 39, pp. 1067-1073
  • Atwell, S., Huang, Y.S., Vilhjálmsson, B.J., Willems, G., Horton, M., Li, Y., Meng, D., Hu, T.T., Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines (2010) Nature, 465, pp. 627-631
  • Baum, S.F., Dubrovsky, J.G., Rost, T., Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots (2002) Am J Bot, 89, pp. 908-920
  • Baxter, I., Hosmani, P.S., Rus, A., Lahner, B., Borevitz, J.O., Muthukumar, B., Mickelbart, M.V., Salt, D.E., Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis (2009) PLoS Genet, 5, pp. e1000492
  • Bouchabke, O., Chang, F., Simon, M., Voisin, R., Pelletier, G., Durand-Tardif, M., Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses (2008) PLoS One, 3, pp. e1705
  • Boursiac, Y., Boudet, J., Postaire, O., Luu, D.T., Tournaire-Roux, C., Maurel, C., Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization (2008) Plant J, 56, pp. 207-218
  • Boursiac, Y., Chen, S., Luu, D.-T., Sorieul, M., van den Dries, N., Maurel, C., Early effects of salinity on water transport in Arabidopsis roots: Molecular and cellular features of aquaporin expression (2005) Plant Physiol, 139, pp. 790-805
  • Bramley, H., Turner, N.C., Turner, D.W., Tyerman, S.D., Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots (2009) Plant Physiol, 150, pp. 348-364
  • Chaumont, F., Moshelion, M., Daniels, M.J., Regulation of plant aquaporin activity (2005) Biol Cell, 97, pp. 749-764
  • Chen, W.J., Chang, S.H., Hudson, M.E., Kwan, W.K., Li, J., Estes, B., Knoll, D., Zhu, T., Contribution of transcriptional regulation to natural variations in Arabidopsis (2005) Genome Biol, 6, pp. R32
  • Christmann, A., Weiler, E.W., Steudle, E., Grill, E., A hydraulic signal in root-to-shoot signalling of water shortage (2007) Plant J, 52, pp. 167-174
  • Collins, N.C., Tardieu, F., Tuberosa, R., Quantitative trait loci and crop performance under abiotic stress: Where do we stand? (2008) Plant Physiol, 147, pp. 469-486
  • Daniels, M.J., Chaumont, F., Mirkov, T.E., Chrispeels, M.J., Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site (1996) Plant Cell, 8, pp. 587-599
  • del Martínez-Ballesta, M.C., Silva, C., López-Berenguer, C., Cabañero, F.J., Carvajal, M., Plant aquaporins: New perspectives on water and nutrient uptake in saline environment (2006) Plant Biol (Stuttg), 8, pp. 535-546
  • Granier, C., Aguirrezabal, L., Chenu, K., Cookson, S.J., Dauzat, M., Hamard, P., Thioux, J.J., Lebaudy, A., PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit (2006) New Phytol, 169, pp. 623-635
  • Henzler, T., Waterhouse, R.N., Smyth, A.J., Carvajal, M., Cooke, D.T., Schaffner, A.R., Steudle, E., Clarkson, D.T., Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus (1999) Planta, 210, pp. 50-60
  • Hirano, Y., Okimoto, N., Kadohira, I., Suematsu, M., Yasuoka, K., Yasui, M., Molecular mechanisms of how mercury inhibits water permeation through aquaporin-1: Understanding by molecular dynamics simulation (2010) Biophys J, 98, pp. 1512-1519
  • Höfer, R., Briesen, I., Beck, M., Pinot, F., Schreiber, L., Franke, R., The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid omegahydroxylase involved in suberin monomer biosynthesis (2008) J Exp Bot, 59, pp. 2347-2360
  • Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S., Kang, H., An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana (2004) Plant Mol Biol, 54, pp. 713-725
  • Javot, H., Lauvergeat, V., Santoni, V., Martin-Laurent, F., Güçlü, J., Vinh, J., Heyes, J., Bouchez, D., Role of a single aquaporin isoform in root water uptake (2003) Plant Cell, 15, pp. 509-522
  • Mahdieh, M., Mostajeran, A., Horie, T., Katsuhara, M., Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants (2008) Plant Cell Physiol, 49, pp. 801-813
  • Martínez-Ballesta, M.C., Aparicio, F., Pallás, V., Martínez, V., Carvajal, M., Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis (2003) J Plant Physiol, 160, pp. 689-697
  • Martre, P., Morillon, R., Barrieu, F., North, G.B., Nobel, P.S., Chrispeels, M.J., Plasma membrane aquaporins play a significant role during recovery from water deficit (2002) Plant Physiol, 130, pp. 2101-2110
  • Matsuo, N., Ozawa, K., Mochizuki, T., Genotypic differences in root hydraulic conductance of rice (Oryza sativa L.) in response to water regimes (2009) Plant Soil, 316, pp. 25-34
  • Maurel, C., Simonneau, T., Sutka, M., The significance of roots as hydraulic rheostats (2010) J Exp Bot, 61, pp. 3191-3198
  • Maurel, C., Verdoucq, L., Luu, D.T., Santoni, V., Plant aquaporins: Membrane channels with multiple integrated functions (2008) Annu Rev Plant Biol, 59, pp. 595-624
  • McKay, J.K., Richards, J.H., Mitchell-Olds, T., Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits (2003) Mol Ecol, 12, pp. 1137-1151
  • McKhann, H.I., Camilleri, C., Bérard, A., Bataillon, T., David, J.L., Reboud, X., le Corre, V., Brunel, D., Nested core collections maximizing genetic diversity in Arabidopsis thaliana (2004) Plant J, 38, pp. 193-202
  • Melchior, W., Steudle, E., Water transport in onion (Allium cepa L.) roots: Changes of axial and radial hydraulic conductivities during root development (1993) Plant Physiol, 101, pp. 1305-1315
  • Miyamoto, N., Steudle, E., Hirasawa, T., Lafitte, R., Hydraulic conductivity of rice roots (2001) J Exp Bot, 52, pp. 1835-1846
  • Munns, R., Passioura, J.B., Hydraulic resistance of plants. III. Effects of NaCl in barley and lupin (1984) Aust J Plant Physiol, 11, pp. 351-359
  • Murashige, T., Skoog, F., A revised medium for rapid growth and bio assays with tobacco tissue cultures (1962) Physiol Plant, 15, pp. 473-497
  • Nienhuis, J., Sills, G.R., Martin, B., King, G., Variance for water-use efficiency among ecotypes and recombinant inbred lines of Arabidopsis thaliana (Brassicaceae) (1994) Am J Bot, 81, pp. 943-947
  • Paquette, A.J., Benfey, P.N., Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORTROOT (2005) Plant Physiol, 138, pp. 636-640
  • Parent, B., Hachez, C., Redondo, E., Simonneau, T., Chaumont, F., Tardieu, F., Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: A transscale approach (2009) Plant Physiol, 149, pp. 2000-2012
  • Poormohammad Kiani, S., Grieu, P., Maury, P., Hewezi, T., Gentzbittel, L., Sarrafi, A., Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.) (2007) Theor Appl Genet, 114, pp. 193-207
  • Postaire, O., Tournaire-Roux, C., Grondin, A., Boursiac, Y., Morillon, R., Schäffner, A.R., Maurel, C., A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis (2010) Plant Physiol, 152, pp. 1418-1430
  • Postaire, O., Verdoucq, L., Maurel, C., Aquaporins in plants: From molecular structure to integrated functions (2007) Adv Bot Res, 46, pp. 75-136
  • Ren, Z., Zheng, Z., Chinnusamy, V., Zhu, J., Cui, X., Iida, K., Zhu, J.K., RAS1, a quantitative trait locus for salt tolerance and ABA sensitivity in Arabidopsis (2010) Proc Natl Acad Sci USA, 107, pp. 5669-5674
  • Rieger, M., Litvin, P., Root system hydraulic conductivity in species with contrasting root anatomy (1999) J Exp Bot, 50, pp. 201-209
  • Siefritz, F., Tyree, M.T., Lovisolo, C., Schubert, A., Kaldenhoff, R., PIP1 plasma membrane aquaporins in tobacco: From cellular effects to function in plants (2002) Plant Cell, 14, pp. 869-876
  • Steudle, E., Water uptake by roots: Effects of water deficit (2000) J Exp Bot, 51, pp. 1531-1542
  • Steudle, E., Peterson, C.A., How does water get through roots? (1998) J Exp Bot, 49, pp. 775-788
  • Törnroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R., Kjellbom, P., Structural mechanism of plant aquaporin gating (2006) Nature, 439, pp. 688-694
  • Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.T., Bligny, R., Maurel, C., Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins (2003) Nature, 425, pp. 393-397
  • Tyerman, S.D., Oats, P., Gibbs, J., Dracup, M., Greenway, H., Turgorvolume regulation and cellular water relations of Nicotiana tabacum roots grown in high salinities (1989) Aust J Plant Physiol, 16, pp. 517-531
  • Vandeleur, R., Niemietz, C., Tilbrook, J., Tyerman, S.D., Role of aquaporins in root responses to irrigation (2005) Plant Soil, 274, pp. 141-161
  • Vandeleur, R.K., Mayo, G., Shelden, M.C., Gilliham, M., Kaiser, B.N., Tyerman, S.D., The role of plasma membrane intrinsic protein aquaporins in water transport through roots: Diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine (2009) Plant Physiol, 149, pp. 445-460
  • Vandesompele, J., de Preter, K., Pattyn, F., Poppe, B., van Roy, N., de Paepe, A., Speleman, F., Accurate Normalization of Real-time Quantitative RTPCR Data By Geometric Averaging of Multiple Internal Control Genes (2002) Genome Biol, 3. , RESEARCH0034
  • Verdoucq, L., Grondin, A., Maurel, C., Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons (2008) Biochem J, 415, pp. 409-416
  • Yu, X., Peng, Y.H., Zhang, M.H., Shao, Y.J., Su, W.A., Tang, Z.C., Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery (2006) Cell Res, 16, pp. 599-608
  • Zimmermann, H.M., Hartmann, K., Schreiber, L., Steudle, E., Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.) (2000) Planta, 210, pp. 302-311
  • Zimmermann, H.M., Steudle, E., Apoplastic transport across young maize roots: Effect of the exodermis (1998) Planta, 206, pp. 7-19

Citas:

---------- APA ----------
Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P. & Maurel, C. (2011) . Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiology, 155(3), 1264-1276.
http://dx.doi.org/10.1104/pp.110.163113
---------- CHICAGO ----------
Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P., Maurel, C. "Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions" . Plant Physiology 155, no. 3 (2011) : 1264-1276.
http://dx.doi.org/10.1104/pp.110.163113
---------- MLA ----------
Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P., Maurel, C. "Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions" . Plant Physiology, vol. 155, no. 3, 2011, pp. 1264-1276.
http://dx.doi.org/10.1104/pp.110.163113
---------- VANCOUVER ----------
Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P., Maurel, C. Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiol. 2011;155(3):1264-1276.
http://dx.doi.org/10.1104/pp.110.163113